Behavioral Ecology Vol. 10 No. 2: 128–135
Aerodynamic costs of long tails in male barn
swallows Hirundo rustica and the evolution of
sexual size dimorphism
Andrés Barbosa and Anders Pape Møller
Laboratoire d’Ecologie, Université Pierre et Marie Curie, CNRS-URA 258, Bât A, 7e étage, 7, quai
Saint Bernard, Case 237, F-75252 Paris, Cedex 05, France
Exaggerated tail feathers of birds constitute a standard example of evolution of extravagant characters due to sexual selection.
Such secondary sexual traits are assumed to be costly to produce and maintain, and they usually are accompanied by morphological adaptations that tend to reduce their costs. The aerodynamic costs for male barn swallows Hirundo rustica of having
long tails were quantified using aerodynamics theory applied to morphological data from seven European populations. Latitudinal differences in tail length were positively correlated with differences in flight costs predicted by aerodynamics theory. A
positive relationship between aerodynamic costs of long tails and the degree of sexual size dimorphism was found among
populations. Latitudinal differences in foraging costs may result in tail length being relatively similar in males and females in
southern populations, whereas the low foraging costs for males in northern populations may allow them to cope with higher
aerodynamic costs, giving rise to large sexual size dimorphism. Enlargement of wingspan in males can alleviate but not eliminate
the costs of tail exaggeration, and therefore differences in aerodynamic costs of male ornaments were maintained among
populations. Sexual size dimorphism in the barn swallow arises as a consequence of latitudinal differences in the advantages of
sexual selection for males and the costs of long tails for males and females. Key words: clinal variation, flight costs, sexual
selection, tail shape. [Behav Ecol 10:128–135 (1999)]
S
econdary sexual characters are more exaggerated than homologous characters in closely related species due to the
effects of sexual selection and its two main components,
male–male competition and female choice (Darwin, 1871).
Sexual selection arises because individuals of the chosen sex
experience advantages over others of the same species and
sex in relation to reproduction. Two different categories of
sexual selection models may account for exaggeration of male
traits. The Fisherian model of mate choice suggests that female preferences coevolve with the male trait, resulting in the
production of exaggerated, attractive, and costly secondary
sex traits (Fisher, 1930). At evolutionary equilibrium this cost
of the secondary sexual character is balanced by its advantages
in terms of increased mating success (Fisher, 1930; Kirkpatrick, 1982; Lande, 1981; Pomiankowski et al., 1991; Sutherland and de Jong, 1991). Alternatively, handicap models assume that the level of signaling adopted by a male is an outcome of individual optimization. Low-quality individuals will
be unable to produce a larger sex trait because the cost of
such a trait is relatively greater for low- than for high-quality
individuals (Andersson, 1986; Grafen, 1990; Heywood, 1989;
Iwasa et al., 1991; Kodric-Brown and Brown, 1984; Price et al.,
1993; Zahavi, 1975). Thus all these models of sexual selection
assume that higher levels of display are prevented because of
the costs of signaling.
Feather ornaments in birds, and particularly extravagant
tails, are standard examples of exaggerated traits that are
maintained by sexual selection. Several experimental studies
of birds demonstrate that males with long tails experience a
Address correspondence to A. Barbosa, who is now at the Departamento de Ecologı́a Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, C/José Gutierrez Abascal, 2, 28006 Madrid, Spain. E-mail:
[email protected].
Received 23 October 1997; revised 29 June 1998; accepted 5 July
1998.
q 1999 International Society for Behavioral Ecology
mating advantage (e.g., Andersson, 1982, 1992; Evans and
Hatchwell, 1992; Møller, 1988) at a viability cost (Evans and
Thomas, 1992; Møller, 1989; Møller and de Lope, 1994;
Møller et al., 1995b; Saino and Møller, 1996; Saino et al.,
1997) and support the hypothesis that sexual selection is the
mechanism responsible for the evolution of long tails (Møller
et al., 1998). Tails of birds are functional units that are shaped
by both natural and sexual selection. Aerodynamics theory
suggests that only the proximal part of the tail until the point
of maximum continuous width is aerodynamically functional
and that any area beyond this point does not increase lift, but
increases drag (Thomas, 1993). Drag is proportional to the
area beyond this point of maximum continuous width, and
such tail drag contributes significantly to the parasite drag of
the bird (Evans and Thomas, 1992; Thomas and Balmford,
1995), which can cause an increase in the power required for
flight (Norberg, 1995). In a forked tail such as that of the
barn swallow Hirundo rustica, the maximum lift for any given
drag is produced by a spread, triangular tail. The optimum
tail shape is one with the outermost tail feathers just slightly
more than twice the length of the central feathers when the
spread tail just exceeds 1208 (Thomas and Balmford, 1995).
An increase in tail length exceeding the optimum ratio of two
would increase tail drag and the power of flight and therefore
increase the cost of flight.
Recently, Norberg (1994) suggested a mechanism that
would improve maneuverability by increasing lift and reducing drag. Basically, tail streamers through aeroelastic properties of distal parts of the feather cause a rotation in their sockets, deflecting the leading edge and acting like certain high
lift devices in aircraft (Norberg, 1994). Evans and Thomas
(1997) predicted from a theoretical study a decrease in turning radius when Norberg’s mechanism was operating. Hence
they suggested that the outermost feathers would not be costly
but would actually confer a natural selection advantage to
males with long streamers. This claim cannot be easily tested
because certain parts of Norberg’s hypothesized mechanism
Barbosa and Møller • Aerodynamic costs and sexual size dimorphism
are difficult to evaluate and relate to improved flight. For example, there is no quantification of the relationship between
the degree of the deflecting leading edge mechanism and the
length of the tail streamer. Obviously, a certain streamer
length causes torsion of the feather, but this torsion could also
be produced by a short streamer, as in females or short-tailed
males. In fact, Norberg (1994) assumed such a possibility, and
although he proposed possible differences in feather characteristics such as flexural stiffness, feather shaft curvature, and
torsional rigidity in relation to the length of the streamer, the
consequences of such differences remain to be demonstrated.
Therefore, the mechanism described by Norberg (1994) does
not make any explicit predictions about the cost of a long tail.
However, there are several pieces of evidence suggesting that
the Norberg effect can be considered a constant acting on the
whole range of tail lengths in barn swallows (Barbosa and
Møller, in press; Møller et al., 1998). A discussion of the effects
of the Norberg mechanism in barn swallows can be found in
Møller et al. (1998) and Barbosa and Møller (in press) and
in the Discussion of the present paper.
Costs of secondary sexual characters can be reduced by the
presence of cost-reducing traits (Møller, 1996). For birds with
elongated tails, elongation and enlargement of wings and narrowing of the outermost tail feathers have been demonstrated
to act as cost-reducing traits (Andersson and Andersson, 1994;
Balmford et al., 1994, Møller et al., 1995a). Although geographical variation in sexual size dimorphism in tail length
and foraging costs have been reported for the barn swallow
(Møller, 1995; Møller and de Lope, 1994; Møller et al.,
1995b), aerodynamical costs sensu stricto of long tails remain
to be quantified.
In this study, we calculated the aerodynamic costs of long
tails in male barn swallows from seven European populations.
We used a theoretical framework to study the relationship between such costs and the degree of sexual dimorphism in tail
length and the size of cost-reducing characters along a latitudinal gradient in size dimorphism. If long streamers in male
barn swallows have evolved by sexual selection, we predicted
a significant positive relationship between costs of long tails
and sexual size dimorphism.
METHODS
Barn swallows are small (approximately 20 g), monogamous,
semicolonial passerine birds that feed on insects caught on
the wing. Sexual size dimorphism is slight with the exception
of the outermost feathers of the forked tail. Male tail length
is only weakly correlated with structural body size, and individual males are highly consistent in tail length among years
(Møller, 1991). Male barn swallows attempt to attract a mate
by performing displays of their tail ornaments in flight or
while perched (Møller, 1988). Female barn swallows visit several males before making their mate choice, and males with
long and symmetrical tails are preferred over ones with short
and asymmetrical tails (Møller, 1988, 1990, 1992a, 1994).
Long-tailed males also experience a number of other sexual
selection advantages (Møller, 1990, 1992b, 1994). Nestlings
are fed by both parents for an average of 3 weeks before fledging.
The studies took place at seven different sites. Kraghede,
Denmark (578 N, 108 E) is an open farmland site with scattered plantations, ponds, and hedgerows. The barn swallows
usually breed on farms either solitarily or in colonies of up to
50 pairs. A detailed description of the population is given in
Møller (1994). Two study sites in the Ukraine were situated
on large cooperative farms in open farmland habitat near
Chernobyl (528 N, 298 E) and Kanev (508 N, 318 E), separated
by a distance of 300 km. The main crops were grass and wheat.
129
Figure 1
Study site cladogram built from differences in latitudinal
coordinates and the increased percentage drag and flight power at
each locality when comparing males with an optimal tail shape and
mean tail length of males.
The barn swallows breed inside stables and cowsheds. The
number of breeding pairs per colony ranged from 20 to 120
pairs. Pärnu, Estonia (588 N, 248 E), is a mixed farmland and
forest habitat with solitary pairs or colonies of up to 50 pairs
of swallows breeding inside stables. The study site at Tiszatelek, Hungary (488 N, 218 E), is an open farmland habitat with
breeding sites at farms having single pairs up to more than
25 pairs. The study site at Milano, Italy (458 N, 98 E), is an
open farmland area. The main crops are maize, grass, wheat,
and soybeans. Fields are bordered by hedges and trees. Barn
swallows breed mainly in cowsheds, milking rooms, garages,
and sometimes outdoors. The number of nests in the colonies
ranged from 18 to 59. The Badajoz, Spain (398 N, 78 W), study
site consists of open farmland with scattered groups of trees
around farms and rivers. The main crops are grass, maize, and
wheat. Barn swallows breed solitarily or colonially (up to 50
pairs) in farmhouses and other buildings.
The distance between study sites and the nearest neighboring site was on average 908 km (SE 5 160, range 300–1500
km, n 5 7). The average natal dispersal of barn swallows is
known to be 0.7 km for males and 2.5 km for females based
on ringing recoveries (Cramp, 1988), and other estimates are
of a similar magnitude (Glutz von Blotzheim and Bauer,
1985). Breeding dispersal is also restricted and rarely exceeds
1 km (Cramp, 1988; Glutz von Blotzheim and Bauer, 1985).
This means that the average distance between study sites is
several hundred times the average natal dispersal distance.
Gene flow between study sites should therefore be minimal
(Endler, 1977; Slatkin, 1985). The statistical dependence of
data from different populations is likely to be related to geographical proximity, and this may affect the reliability of statistical analyses in a similar way to phylogenetic analyses (Felsenstein, 1985). To avoid this problem, we adopted the independent contrast method using geographical distance as an
estimate of genetic divergence between populations based on
an assumption of isolation by distance. As geographic variation in most morphological traits of the barn swallow shows a
latitudinal cline (Møller, 1995), we built a cladogram based
on latitudinal coordinates of each study site (Figure 1), using
the unweighted pair-group average method (UPGM; James
and McCulloch, 1990; Sneath and Sokal, 1973). Statistical analyses of relations between characters were determined using
contrasts derived from the geographical distance cladogram.
These contrasts were calculated as the value of a trait (e.g.,
tail dimorphism) in one population (or node) of the clado-
Behavioral Ecology Vol. 10 No. 2
130
Table 1
Morphological measurements of males of different barn swallows populations (means 6 SE)
Population
Wing span (mm)
Badajoz
Milano
Tiszatelek
Kanev
Chernobyl
Kraghede
Pärnu
321.73
322.03
335.07
324.59
330.74
329.10
328.71
6
6
6
6
6
6
6
0.83
0.44
0.91
0.39
0.82
0.03
3.03
Tail length (mm)
97.86
104.48
112.18
109.75
107.68
107.48
110.36
6
6
6
6
6
6
6
1.39
0.58
1.43
0.99
1.45
0.30
1.43
gram subtracted from the value of the closest population (or
node). Thus each population or node was compared to its
closest population. Euclidean distances were used as branch
lengths in contrast analyses because Felsenstein’s method requires knowledge of branch lengths in the cladogram (see
Felsenstein, 1985, for more details). To be able to identify
covariation between variables, regression through the origin
was used to test the relationship (Garland et al., 1992). To
make unique representations of bivariate scatterplots, one
must set all contrasts for one trait (e.g., the independent variable) positive, while switching signs for the other trait’s corresponding contrasts. Regression through the origin yields the
same results whether contrasts are thus positivized (Garland
et al., 1992).
Most adult barn swallows were captured in mist nets at the
breeding sites. All birds were provided with a numbered aluminium band to allow identification. Individuals were sexed
from the presence (females) or absence (males) of a brood
patch and by the shape of the cloacal protuberance (Svensson, 1984).
Morphological characters (Table 1) were measured by
A.P.M. (Kraghede, Pärnu, Chernobyl, Kanev) or using exactly
the same methods by other field workers given instructions by
A.P.M. in order to reduce interobserver variability. However,
we included the person who took the measurements as a dummy variable (0 for other persons, 1 for A.P.M.) to test whether
interobserver variability had affected the results. The morphological characters were used as dependent variables in
multiple linear regression analyses with latitude, the person
dummy variable, and the latitude-person variable interaction
as independent variables. None of the regression coefficients
for the dummy variable or the interaction were statistically
significant (p . .05), which suggests that variation in morphology along the latitudinal gradient was unbiased by the
person who had taken the measurements.
The length of the outermost tail feathers, hereafter called
tail length, and the central tail feathers were measured with
a ruler to the nearest millimeter. We measured wing span to
the nearest millimeter as the distance between wing tips when
the wings were stretched maximally. Body mass was recorded
to the nearest 0.1 g using a Pesola spring balance. We determined sexual size dimorphism in tail length as the residuals
from a regression of mean values for males regressed on mean
values for females in each population. The regression was statistically highly significant and positive [male tail length 5 51
1 0.36 (female tail length), F 5 18.57, df 5 1,5, r 5 .88, p 5
.007].
To calculate tail drag and power curves of power consumption in each population, we used the mean tail length and
the hypothetical optimum tail length for each population in
the aerodynamic models (tail length divided by central feather length equaling two; Thomas and Balmford, 1995). The
tail was assumed to have a triangular shape with streamers in
Central tail length (mm) Body mass (g)
42.76
44.89
47.83
44.08
44.68
44.31
43.12
6
6
6
6
6
6
6
0.18
0.11
0.24
0.24
0.35
0.008
0.27
18.44
18.52
19.46
18.30
18.63
19.14
19.03
6
6
6
6
6
6
6
0.17
0.09
0.13
0.12
0.18
0.04
0.18
Sample size
55
212
54
69
50
856
41
the former case and a triangular tail without streamers projecting beyond the maximum continuous span in the latter
case. The Norberg effect has been considered constant because there is no empirical evidence of differential effects
among different individuals (Barbosa and Møller, in press;
Møller et al., 1998; see also Norberg, 1994).
Tail drag calculations were performed using the formula
from Prandtl and Tietjens (1934) for a flat plate with Reynolds
number less than 106 (Evans and Thomas, 1992)
Drag 5 0.6635rsÏlvu3
where r 5 1.23 (kg/m3) is the density of air, s is tail span, l
is tail length, v 5 1.45 3 1025 (m2s21) is the kinematic viscosity
of air, and u is velocity.
Power curves of power consumption were calculated using
a modified version of the computer programs in Pennycuick
(1989) adding tail drag. We used Pennycuick’s model because
it provides the most realistic estimate of flight costs in comparison with other aerodynamic models (Welham, 1994; see
also Evans and Thomas, 1992). This model allows calculations
of aerodynamic performance in relation to flight speed on
the basis of body mass and wingspan of birds (Pennycuick,
1989).
Increases in power consumption and drag due to tail length
in each population were calculated as the percentage increase
for the mean tail length with respect to the hypothetical optimum tail length (see above). The increase in wingspan needed to compensate for the flight costs due to tail elongation
were calculated. Wingspan values were manipulated in the
computer models until flight costs at the mean speed considered for a bird with an elongated tail were the same as for a
bird with the optimal tail length.
Latitudinal variation in tail length has been related to latitudinal variation in foraging costs (Møller et al., 1995a). We
have explored the possible variation in such a foraging costs
comparing the size of prey available for barn swallows with
the size of prey captured by barn swallows at different latitudes. We have compared the percentage increase of mean
size between available prey and selected prey in the three populations for which this kind of data were available (Kraghede,
578 N, Møller AP, unpublished data; Stirling, 568, Turner,
1980; Lippstadt, 518, Loske, 1993).
RESULTS
Table 2 shows differences in drag at different flight speeds
between optimal and elongated tails in the seven populations
of barn swallows. Assuming a mean flight speed of barn swallows to be about 10 m/s (Harrison, 1931; Meinertzhagen,
1955), the percentage increase of drag in males with a long
tail in relation to the hypothetical optimum tail length ranged
from 7.0% in the Badajoz population to 15.3% in the Pärnu
population (Figure 1). The effect of increase in drag due to
Barbosa and Møller • Aerodynamic costs and sexual size dimorphism
131
Table 2
Calculated drag (1023 Newton) from aerodynamics theory of the optimum (Opt) tail length (see Methods) and of mean tail length in male
barn swallows from seven European populations
Air
speed
(m/s)
Opt
Mean
Opt
3
4
5
6
7
8
9
10
0.6999
1.0776
1.5061
1.9798
2.4948
3.0481
3.6372
4.2599
0.7487
1.1528
1.6111
2.1178
2.6688
3.2606
3.8907
4.5569
0.7526
1.1587
1.6193
2.1286
2.6824
3.2773
3.9106
4.5801
Badajoz
Milano
Tiszatelek
Kanev
Mean
Opt
Mean
Opt
0.8122
1.2505
1.7476
2.2973
2.8950
3.5370
4.2205
4.9431
0.8275
1.2741
1.7806
2.3407
2.9497
3.6038
4.3002
5.0365
0.8962
1.3797
1.9283
2.5348
3.1942
3.9026
4.6567
5.4541
0.7326
1.1279
1.5763
2.0721
2.6112
3.1903
3.8068
4.4586
long tails relative to the optimal tail length on power of flight
is shown in Table 3. At the mean speed considered, the percentage of power increase with respect to the optimum tail
length ranged from 0.9% in the Badajoz population to 1.5%
in the Kanev population (Figure 1). Mean percentage of drag
and flight power increase between optimal and long-tailed
phenotypes was 10.2% and 1.3%, respectively.
The results did not change using the independent contrast
method instead of the species regression which considers each
population to contribute a statistically independent data
point. However, we present the results for the independent
contrast method to correct for any possible effects of independence due to geographical proximity.
The increase in tail drag and flight power were significantly
positively related to sexual size dimorphism in the seven populations [b (SE) 5 0.84 (0.24), t 5 3.47, df 5 5, p 5 .01; b
(SE)5 0.80 (0.26), t 5 3.01, df 5 5, p 5 .02; Figure 2). The
percentage increase in wingspan was positively, but not significantly, related to the percentage increase in tail elongation
[b 5 0.72 (0.30), t 5 2.34, df 5 5, p 5 .06; Figure 3].
Table 4 shows the percentage difference in mean prey size
captured relative to the available prey in the three populations. Northern populations selected much larger prey with
respect to the size available than southern populations, consistent with a decrease in foraging costs toward the north.
DISCUSSION
Exaggeration of secondary sexual characters such as tail feathers is costly according to current models of sexual selection
(Andersson, 1986; Fisher, 1930; Grafen, 1990; Heywood, 1989;
Iwasa et al., 1991; Pomiankowski et al., 1991; Zahavi, 1975). A
Chernobyl
Kraghede
Pärnu
Mean
Opt
Mean
Opt
Mean
Opt
Mean
0.8174
1.2585
1.7588
2.3120
2.9135
3.5596
4.2475
4.9747
0.7476
1.1510
1.6085
2.1145
2.6646
3.2555
3.8846
4.5497
0.8206
1.2588
1.7657
2.3211
2.9250
3.5737
4.2642
4.9944
0.7383
1.1367
1.5886
2.0883
2.6316
3.2152
3.8365
4.4934
0.8131
1.2518
1.7495
2.2998
2.8991
3.5408
4.2251
4.9484
0.7085
1.0908
1.5245
2.0040
2.5753
3.0853
3.6815
4.3119
0.8015
1.2339
1.7245
2.2689
2.8567
3.4902
4.1647
4.8777
number of different costs of elongated tails have been reported. Møller (1989) and Møller and de Lope (1994) provided experimental evidence for the presence of a considerable viability cost of long tails in male barn swallows. Longtailed males were better able to survive tail elongation, whereas short-tailed males survived relatively better when their tails
were shortened. Foraging costs of tail exaggeration have also
been reported in barn swallows (Møller, 1989; Møller and de
Lope, 1994; Møller et al., 1995a): males with experimentally
elongated tails captured more and smaller prey than tail-shortened individuals, but males with naturally long tails were less
affected by experimental treatment. Optimal prey for the
barn swallow are large, actively flying insects according to optimal foraging models (Bryant and Turner, 1982; Turner,
1982), but these prey are difficult to catch for long-tailed
males, both with naturally and experimentally elongated tails
(Møller, 1992b; de Lope and Møller, 1993; Møller et al.,
1995a). Direct aerodynamic costs of long tails have been demonstrated a few times. Evans and Thomas (1992) showed that
malachite sunbirds (Nectarinia johnstoni) with experimentally
elongated tails spent less time flying than before manipulation. The theoretical aerodynamic effects of tail elongation
have been analyzed for bird species with different tail morphologies (Balmford et al., 1993; Norberg, 1995; Thomas,
1993; Thomas and Balmford, 1995). Here we calculated the
aerodynamic costs (in terms of increased drag and flight power) of tail elongation in male barn swallows from seven European populations and investigated how such costs were related to sexual size dimorphism, geographical variation in dimorphism, and the presence of cost-reducing morphological
traits.
Table 3
Calculated flight power (W) from aerodynamics theory for the optimum (Opt) tail length (see Materials and Methods) and mean tail length
in male barn swallows from seven European populations
Air
speed
(m/s)
Badajoz
Opt
Mean
Opt
3
4
5
6
7
8
9
10
0.206
0.196
0.198
0.209
0.229
0.258
0.297
0.346
0.206
0.196
0.198
0.210
0.230
0.259
0.299
0.349
0.207
0.197
0.199
0.211
0.231
0.261
0.300
0.350
Milano
Tiszatelek
Kanev
Mean
Opt
Mean
Opt
0.207
0.198
0.200
0.212
0.232
0.263
0.303
0.354
0.213
0.203
0.205
0.217
0.239
0.270
0.311
0.364
0.213
0.203
0.206
0.219
0.241
0.272
0.315
0.433
0.201
0.192
0.194
0.206
0.226
0.255
0.294
0.344
Chernobyl
Kraghede
Pärnu
Mean
Opt
Mean
Opt
Mean
Opt
Mean
0.202
0.193
0.195
0.207
0.228
0.258
0.298
0.349
0.202
0.193
0.195
0.207
0.228
0.258
0.297
0.347
0.202
0.193
0.196
0.208
0.230
0.260
0.301
0.352
0.212
0.202
0.203
0.215
0.236
0.265
0.305
0.356
0.212
0.202
0.204
0.216
0.237
0.268
0.309
0.361
0.210
0.200
0.202
0.213
0.233
0.263
0.303
0.353
0.211
0.201
0.203
0.215
0.236
0.266
0.307
0.358
Behavioral Ecology Vol. 10 No. 2
132
Figure 3
Relationship between contrasts of male tail length and contrasts of
theoretical wingspan increase to reduce flight costs.
Figure 2
Relationships between (A) contrasts of increase in drag and
contrasts of flight power and (B) contrasts of sexual size
dimorphism among barn swallow populations.
The optimal tail shape for an aerially foraging bird with a
forked tail that gives rise to the maximum lift-to-drag ratio is
one that forms a triangular platform and a straight trailing
edge when the tail is spread at an angle of approximately 1208
(Thomas, 1993). The outermost tail feathers will then be twice
the length of the central tail feathers. Male barn swallows in
all seven populations had outermost tail feathers that on average were much longer than twice the length of the central
tail feathers (see also Møller, 1995; Møller et al., 1995b). Such
elongation increases costs because any area beyond the point
of maximum continuous width of the tail does not increase
lift but increases drag (Thomas, 1993). Overcoming drag is
the major energetic cost of flight (Gill and Wolf, 1975). Energy expenditure on locomotion cannot be used for other
demanding activities such as an efficient immune system, and
the energy cost of ornament exaggeration thus imposes a reduction in the amount of resources available for immune
function (König and Schmid-Hempel, 1995; Saino and Møller,
1996).
Flight costs are affected by the different degree of tail elongation of males in different populations of barn swallows (Tables 2 and 3), increasing with latitude (Figure 1). Tail length
manipulation affects flight costs and foraging efficiency, which
may give rise to the observed reduced survival of male barn
swallows with experimentally elongated tails and the increased
survival of males with shortened tails (Møller, 1989; Møller
and de Lope, 1994). The cost of barn swallow tail ornaments
may vary geographically if ambient temperature affects insect
physiology and thereby the energy cost of prey capture. Flight
performance of insects, including their ability to escape avian
predators, depends on ambient temperature (Beament and
Treherne, 1968; Taylor, 1963; Wigglesworth, 1972). Barn swallows are specialist predators of large, actively flying Diptera
that constitute the optimal diet (Bryant and Turner, 1982).
Large insects are more difficult to catch at the higher temperatures that predominate at southern latitudes, as shown by
Møller et al. (1995a). Geographic variation in the mean size
of insect prey captured by barn swallows relative to the mean
size available is consistent with a latitudinal trend in foraging
costs (Table 4). Although foraging costs decrease with increasing insect abundance due to a reduction in the cost of searching for a new prey, the cost of prey capture per item will be
unaffected by prey abundance. Prey-searching flight does not
require the same maneuverability and agility as that of prey
capture because it consists of rapid flight with the tail furled
and therefore has little aerodynamic cost (Thomas, 1996).
Our aerodynamic analyses are thus consistent with an eco-
Table 4
Mean size of available insect prey and mean size of prey captured by adult barn swallow in three
different populations
a
Population
Mean size of
available prey
Mean size of
taken prey
% Size increase
between available
and captured prey
Kraghede (578 N)
Stirling (568 N)
Lippstadt (518 N)
4.8 mm
2.21 g
3.6 mm
10.6 mm
6.61 g
4.8 mm
120
44a
33
The percentage increase for Stirling was calculated based on the cube-root of the mass of insects.
Barbosa and Møller • Aerodynamic costs and sexual size dimorphism
133
morphological relationship between aerodynamic costs due to
tail elongation and the difficulty of capturing insects. The lowest flight costs are found in southern populations in which
foraging costs are the highest due to superior insect flight
performance. Aerodynamic costs increase with latitude and
are the highest in populations where insects can readily be
caught. Therefore, there appears to be a trade-off between
foraging costs and aerodynamic costs affecting the size of tail
ornaments in male barn swallows.
Geographic variation in sexual size dimorphism in barn
swallows has been explained by geographic variation in the
costs of long tails for the two sexes (Møller, 1995). We found
a positive relationship between aerodynamic costs of long tails
and the degree of sexual size dimorphism among populations
(Figure 2), suggesting that long tails in males have evolved by
sexual selection. As shown above, aerodynamic costs during
foraging enforce the tail morphology of males at southern
latitudes to be close to the aerodynamic optimum and therefore close to the morphology of female tails. At high latitudes,
where foraging costs are low, males are less constrained, and
they can cope with higher aerodynamic costs, and larger differences in sexual size dimorphism thus evolve (see also
Møller, 1995).
Our previous arguments have only considered males. However, the evolution of sexual size dimorphism is a process governed by the differential effects of natural and sexual selection on individuals of the two sexes. Although there is a slight
latitudinal increase in tail length in females, this is considerably less than the increase in males (Møller, 1995), presumably because long tails are more costly for females than for
males. Tail elongation in females has been suggested to be a
consequence of a correlated response to sexual selection on
males (Cuervo et al., 1996) because of a strong positive genetic correlation between the sexes (Møller, 1993). Thus geographic variation in sexual size dimorphism in the barn swallow seems to arise as a consequence of foraging costs of long
tails in both sexes, allowing little divergence at southern latitudes, but more divergence in cold climates, where large dipteran prey are relatively easily captured even by long-tailed
males.
Recently, Norberg (1994) proposed a hypothetical mechanism for increasing lift by the barn swallow tail due to the
distal feather bending upward and backward with the torsion
of the feather deflecting the leading edge. This mechanism
was suggested to provide an explanation based on natural selection for the evolution of tail streamers in the barn swallow
(Evans and Thomas, 1997; Norberg, 1994; Thomas and Rowe,
1997). Norberg’s paper only describes a possible mechanism
that relates feather bending and feather torsion to increased
lift. Norberg does not present data demonstrating that such
relationships are dependent on tail length. The functional relationship between streamer length and the degree of deflection of the leading edge of the tail remains to be determined.
Moreover, differential lift related to different degrees of deflection also remains to be demonstrated. The unknown relationship between the different parameters involved in the
Norberg mechanism makes the effect difficult to assess. Aerodynamic calculations can only include Norberg’s mechanism
when the relationship between streamer length, the degree
of distal feather bending (upward and backward), the degree
of feather torsion, and the amount of lift achieved have been
quantified. However, several pieces of evidence suggest that
the Norberg effect is independent of streamer length and that
the mechanism acts for short streamers such as those of female barn swallows or those of species of hirundines with shallow, forked tails (Norberg, 1994). Norberg (1994) assumed
that even without streamers, it would be possible to achieve a
similar effect to improve flight (see also Møller et al., 1998;
Barbosa and Møller, in press).
The following evidence suggests that the Norberg mechanism is unrelated to the length of tail feathers. First, differences in the length of streamers of male and female barn
swallows are unrelated to differences in the flight costs of each
sex (Barbosa et al., submitted). Second, the probability of
feather damage is positively correlated with tail length in male
barn swallows, increasing the flight costs for long-tailed individuals due to the effects of tail asymmetry on flight performance (Barbosa et al., submitted). Third, there are differences in the evolution of deep and shallow forked tails in hirundines (Barbosa and Møller, unpublished data). Fourth, sexual
size dimorphism in juveniles during the first winter cannot be
explained by Norberg effect because the outermost tail feathers do not extend beyond the central feathers when the tail
is spread at 1208. The ratio of the length of the outermost tail
feathers to that of the central feathers is on average 1.55 in
juvenile males and 1.47 in juvenile females (Cadée et al., submitted). Therefore, it is unlikely that sexual size dimorphism
in juveniles is explained by natural selection through the Norberg effect. Instead, sexual size dimorphism in juveniles could
be explained in the light of sexual selection acting on adult
dimorphism. Finally, Norberg assumed a relationship between
feather traits such as the feather shaft, curvature, and flexion
stiffness, but, as stated above, these hypothetical relations remain to be tested. Furthermore, if the Norberg mechanism
was dependent on tail length, we should expect streamer
length to be related to the functional part of the outermost
tail feather. However, we have determined the relationship
between streamer length and basal feather length and found
no association in either sex in five different populations of
barn swallows (Barbosa and Møller, unpublished data). These
results also suggest that the deflecting leading edge mechanism is not determined by the relation between basal feather
length and streamer length.
Several studies have shown that the presence of costly secondary sex traits often results in the evolution of cost-reducing characters (see review in Møller, 1996). Aerodynamic costs
due to tail elongation can be reduced by an enlarged wingspan (Thomas, 1993). Birds with exaggerated tail ornaments
have longer wings than closely related species without ornaments (Andersson and Andersson, 1994; Balmford et al.,
1994). Male barn swallows have reduced the aerodynamic
costs of their outermost tail feathers by increased wingspans
and a reduced width of the outermost tail feathers (Møller et
al., 1995b). Our analyses show that there is a positive, but not
significant, relationship between the increase in wing length
needed to reduce the flight costs and the degree of sexual
size dimorphism among barn swallow populations (Figure 3).
However, despite such cost reduction, a flight cost of long tails
in males still remains, as indicated by differences in flight costs
among populations.
In conclusion, long tail streamers of male barn swallows entail aerodynamic costs that are reduced by the presence of
cost-reducing characters such as an increased wingspan. Geographical differences in male tail length and their inherent
aerodynamic costs are constrained by foraging costs that are
responsible for geographic differences in sexual size dimorphism.
F. de Lope, N. Saino, M. Kose, and T. Szep kindly helped collecting
data. A.P.M. was supported by grants from the Swedish and Danish
Natural Science Research Councils. A.B. was supported by a Marie
Curie postdoctoral grant of the European Communities
(ERB4001GT951093). Anders Hedenström kindly reviewed a first version of the manuscript and made helpful suggestions. T. Garland
134
kindly provided the programs for calculations of independent contrasts.
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